Adaptive changes in smooth pursuit eye movements induced by cross-axis pursuit-vestibular interaction training in monkeys

The smooth pursuit system interacts with the vestibular system to maintain the accuracy of eye movements in space. To understand neural mechanisms of short-term modifications of the vestibulo-ocular reflex (VOR) induced by pu rsuit-vestibular interactions, we used a cross-axis procedure in trained mo nkeys. We showed earlier that pursuit training in the plane orthogonal to t he rotation plane induces adaptive cross-axis VOR in complete darkness. To further study the properties of adaptive responses, we examined here the in itial eye movements during tracking of a target while being rotated with a trapezoidal waveform. (peak velocity 30 or 40 degrees /s). Subjects were he ad-stabilized Japanese monkeys that were rewarded for accurate pursuit. Who le body rotation was applied either in the yaw or pitch plane while present ing a target moving in-phase with the chair with the same trajectory but in the orthogonal plane. Eye movements induced by equivalent chair rotation w ith or without the target were examined before and after training. Before t raining, chair rotation alone resulted only in the collinear VOR, and smoot h eye movement-tracking of orthogonal target motion during rotation had a n ormal smooth pursuit latency (ca 100 ms). With training, the latency of ort hogonal smooth tracking eye movements shortened, and the mean latency after 1 h of training was 42 ins with a mean gain, at 100 ms after stimulus onse t, of 0.4. The cross-axis VOR induced by chair rotation in complete darknes s had identical latencies with the orthogonal smooth tracking eye movements , but its gains were < 0.2. After cross-axis pursuit training, target movem ent alone without chair rotation induced smooth pursuit eye movements with latencies ca 100 ins. Pursuit training alone for 1 h using the same traject ory but without chair rotation did not result in any clear change in pursui t latency (ca 100 ms) or initial eye velocity. When a new target velocity w as presented during identical chair rotation after training, eye velocity w as correspondingly modulated by just 80 ms after rotation onset, which was shorter than the expected latency of pursuit (ca 100 ms). These results ind icate that adaptive changes were induced in the smooth pursuit system by pu rsuit-vestibular interaction training. We suggest that this training facili tates the response of pursuit-related neurons in the cortical smooth pursui t pathways to vestibular inputs in the orthogonal plane, thus enabling smoo th eye movements to be executed with shorter latencies and larger eye veloc ities than in normal smooth pursuit driven only by visual feedback.